Introduction

The acromioclavicular (AC) joint provides a structural connection between the scapula and the clavicle, which facilitates support of the upper extremity on the thorax. To date, several reports have been published that dealt with the degenerative features of the AC joints. According to DePalma [3], degeneration of the AC joint is a natural consequence of aging, and has been noted to commence in the second decade. Edelson [4] investigated the pattern of degenerative changes of AC joints in 280 dry bone skeletons. They described that there was a consistent pattern of degeneration of this joint; an anteroposterior elongation of the joint was observed on the acromial side, whereas a broadening and rounding of the distal clavicle in the anteroposterior direction was observed on the clavicular side. On the other hand, inferior projecting osteophytes also appeared during the progression of osteoarthritis of the AC joint. Several authors have implicated the role of these inferior pathologies in the development of impingement syndrome [2, 20].

The three-dimensional motions of the AC joint have also been investigated in the previous studies. Worcester and Green [20] described three types of motions at this joint, such as anteroposterior gliding, hinge-like tilting of the scapula on the clavicle and rotation about the long axis of the clavicle. Afterward, several authors investigated more detailed AC joint kinematics during shoulder motion using advanced technique, including the three-dimensional electromagnetic tracking systems [11, 13] and MR imaging [7, 16]. These studies revealed that various types of motions with considerably large degrees occurred in this joint with shoulder motions. Such complex motions may cause inhomogeneous and regional attrition within the joint. In other words, the extent of histological degeneration may reflect the regional differences of the applied biomechanical stresses to the joint surface over a long time period. However, it has not been fully clarified yet the localization pattern of its histological degeneration.

In the present study, we evaluated the histological features of AC joints using cadaveric specimens. Particularly, we focused on the localization of the degenerative changes on the articular cartilage as well as the intraarticular disc.

Materials and methods

A total of 38 AC joints (22 males and 16 females) were harvested from 24 embalmed cadavers. Their mean age at the time of death was 81 years (range 69–91 years). Each specimen was prepared for the present study by cutting both the acromion and clavicle 2–3 cm from the joint space. All muscular attachments including the deltoid, pectoralis major, and trapezius were carefully removed not to damage the joint capsule. After decalcification, each specimen was sectioned into four equal-thickness pieces in the coronal plane (Fig. 1). Consequently, sections at three different cutting surfaces (anterior, middle and posterior) were obtained for each specimen, which were stained with hematoxylin and eosin, and with safranin O, fast green and iron hematoxylin.

Fig. 1
figure 1

Macroscopic findings of the cut surface of the acromioclavicular (AC) joint. The AC joint was sectioned into four equal-thickness pieces in the coronal plane. Three different cutting surfaces (anterior, middle and posterior) were assessed histologically in each specimen

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To evaluate the regional differences in the articular cartilage, both the acromion and the distal end of the clavicle were divided into upper and lower halves (A: the upper part of the acromion, A′: the lower part of the acromion, C: the upper part of the distal end of the clavicle, and C′: the lower part of the distal end of the clavicle) (Fig. 2). The histological features in each part were assessed separately as described below (Fig. 3).

Fig. 2
figure 2

Division of the articular cartilage into four parts. The articular cartilage of the acromion and that of the distal end of the clavicle were divided into upper and lower halves, respectively. A The upper half of the acromion, A′ the lower half of the acromion, C the upper half of the distal end of the clavicle, and C′ the lower half of the distal end of the clavicle

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Fig. 3
figure 3

Histological features in the middle section of the AC joint (72-year-old male, hematoxylin-eosin staining, ×100). For both the acromion and the distal end of the clavicle, the articular cartilage was thinner in the lower half (A′, C′) than in the upper half (A, C) (black arrows). The tidemark was damaged severely in the lower part of the joint (A′, C′) due to the presence of infiltrated inflammatory cells and the blood vessels (white arrow heads)

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Articular cartilage

Image J (version 1.42, http://rsbweb.nih.gov/ij) software was used for the image analysis. The total area of cartilaginous tissue (S: mm2) as well as the entire width of cartilage (W: mm) was measured, and the mean cartilage thickness (S/W: mm) was established for each section. Then, the mean cartilage thickness was compared between the upper and lower halves for both acromin (A to A′) and distal clavicle (C to C′), in order to clarify the superoinferior difference. Moreover, the values obtained from the same half (upper or lower) were also compared among three sections (anterior, middle and posterior sections) for evaluating the anteroposterior differences of cartilage thickness.

To assess the extent of degenerative changes in the articular cartilage, staining property with safranin O was graded using the grading system proposed by Mankin et al. [10]; normal as 0, slight reduction as 1, moderate reduction as 2, severe reduction as 3, and no dye noted as 4. The extent of tidemark integrity in each section was graded on a scale of zero to three; the intact tidemark in the entire section was scored as 0, the damaged (multilayered or indistinct) tidemark including less than a quarter of each section as 1, the damage to less than half as 2, and the damage to more than half as 3. Then, the grades obtained from the upper and lower halves for both acromion and distal clavicle were compared to clarify the difference of degenerative changes at the superoinferior plane. In addition, the anteroposterior difference was also evaluated by comparing the grading scores from the same part (upper or lower) among three sections (anterior, middle and posterior).

Intraarticular disc

Interposed tissues between the AC joint were also evaluated, focusing on their shapes and histological features. Regarding the shape of the disc of the AC joint, DePalma [3] and Salter et al. [17] described two representative types: a complete disc and a meniscoid-like disc. Based on these reports, we classified the shape of the disc into the following three types: complete, meniscoid-like, and absent discs. Histologically, the disc tissue was also divided into the upper and lower parts, which were classified separately into the following two subtypes: fibrocartilaginous subtype and fibrous subtype with granulation tissues.

In addition, we attempted to clarify whether the intraarticular disc played some roles to protect the articular cartilage or not. To answer this question, the cartilage thickness was compared between the specimens with a disc and those without a disc in each part (A, A′, C and C′).

Statistical analyses

Paired t test was used to determine the difference of the mean thickness of articular cartilage in each bone. Wilcoxon paired test was used for the graded scores including the staining property with safranin O as well as the tidemark integrity between upper and lower halves.

To assess the difference among three sections (anterior, middle and posterior), one-way analysis of variance was used for the mean thickness of articular cartilage, whereas the Friedman test was used for the grading scores (the safranin O staining and the tidemark integrity).

Statistical analyses were performed using the software, GraphPad Prism (version 5.0, San Diego, CA, USA). The level of significance was set at p = 0.05.

Results

Articular cartilage

The measured thickness of the articular cartilage for A, A′, C, and C′ in 38 joints was shown in Table 1. For both the acromion and the distal end of the clavicle, the articular cartilage was notably thinner in the lower half than in the upper half (p < 0.01). On the other hand, there were no significant differences in the mean cartilage thickness among the anterior, middle and posterior sections.

Table 1 The measured thickness of the articular cartilage, values and median (range)
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In most of the specimens, the articular cartilage demonstrated a considerable reduction of safranin O staining (Fig. 4). Such reduction of the staining property was more evident in the lower half of the AC joint than in the upper half. Particularly in the lower half of the AC joints (A′ and C′), the anterior section represented less reduction of safranin O staining property than the middle or posterior sections.

Fig. 4
figure 4

Histological assessment of the staining property with safranin O. The reduction of the staining property with safranin O was significantly more evident in the lower half than in the upper half except for the acromial side of articular cartilage in the anterior section. In the lower half of the AC joints (A′ and C′), the anterior section represented less reduction of the staining property than the middle or posterior sections. *Wilcoxon paired test between superior and inferior halves of cartilage thickness. **Friedman test for three sections (anterior, middle and posterior)

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The tidemark in the articular cartilage represented more extensive damage in the lower half than in the upper half (p < 0.05, Fig. 5), similarly to the reduction of the staining property with safranin O. However, no significant differences for the tidemark integrity were shown when comparing among the anterior, middle and posterior sections.

Fig. 5
figure 5

Histological assessment of the tidemark integrity. The tidemark in the lower half was significantly more damaged (multilayered or indistinct) than that in the upper half. *Wilcoxon paired test between superior and inferior halves of cartilage thickness

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Intraarticular disc

Among 38 joints examined in the present study, no specimens displayed a complete disc, which divided the joint space into two different compartments (Table 2). Twenty-nine joints demonstrated a meniscoid-like wedge-shaped disc, whereas, no interposed tissues were observed in nine joints.

Table 2 The shapes and histological features of the intraarticular discs
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Regarding the histological features, the upper part of the disc underneath the superior joint capsule predominantly consisted of the fibrocartilaginous tissue (21 of 27 joints). On the other hand, the lower part of the disc that attached to the inferior joint capsule mainly consisted of the fibrous tissues with granulation (24 of 26 joints).

As for the cartilage thickness, no significant differences were found between the specimens with a disc and those without a disc both for the upper and lower parts of the joint (Fig. 6). It seemed that the presence or absence of the intraarticular discs may not affect the thickness of the cartilage.

Fig. 6
figure 6

Cartilage thickness in the specimens with and without an intraarticular disc. White and black bars represent the mean cartilage thickness (mm) and error bars show their standard deviations (A the upper half of the acromion, A′ the lower half of the acromion, C the upper half of the distal end of the clavicle, and C′ the lower half of the distal end of the clavicle)

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Discussion

The present study demonstrated that the articular cartilage in the lower half of the AC joint was more degenerated than that in the upper half. The localization pattern of the histological degeneration in the articular cartilage might reflect the regional difference in the biomechanical stresses applied to the joint over a long time period. It was known that several types of motions occurred at the AC joint, including gliding and hinge-like tilting of the scapula on the clavicle, and rotation about the long axis of the clavicle [7, 11, 16, 20]. Especially, the rotational motion, in conjunction with shear force and high compressive force produced by the deltoid, was believed to contribute to the development of degenerative diseases of the joint [1, 14]. Anatomically, the AC joint was known to be stabilized by the superior, inferior, anterior, and posterior AC capsular ligaments [6]. Particularly, Klimkiewicz et al. [9] reported that the superior AC ligament played the greatest role among these four ligaments to obtain the stability of this joint. Therefore, the AC joint seemed to rotate around the superior AC ligament, which might cause a marked shearing stress on the inferior part of the articular cartilage.

On the other hand, the extent of the degeneration in the articular cartilage was not varied significantly between anterior, middle and posterior sections except the staining property of safranin O. Based on these results, we assumed that the mechanical stresses applied on this joint might not be varied greatly between its anterior and posterior parts.

Regarding the intraarticular disc, Salter et al. [17] described that the meniscoid-like wedge-shaped discs were most frequently seen in the human cadaveric AC joints. They also found that some specimens represented only a remnant of the disc or entirely absent due to degenerative changes of the joint. In the present study, we confirmed their findings with regard to the shape of the intraarticular disc. Histologically, we found that the upper part of the disc tended to be fibrocartilaginous, while the lower part mainly consisted of loose, fibrous tissue with granulation. In other words, degenerative changes of the disc were also more advanced in the lower part of the AC joint. Ernberg and Potter [5] suggested that the failure of the disc accommodated the incongruent joint surfaces, which might lead cartilage to further degenerative changes. Therefore, repetitive mechanical stress to the AC joint is likely to affect the lower part of the disc, as well as the articular cartilage.

There were several limitations in the present study. First, no clinical information was available for the cadavers used in the present study, including their shoulder symptoms or traumatic histories. We could not investigate the relationship between the history of the cadavers and the results of the histological assessments. Second, the number of specimens was limited, all of which were from elderly donors. Thus, our results could not entirely explain the age-related cartilage changes in the human AC joints. Since, however, the main goal of the present study was to investigate the localization of degenerative changes within the joint rather than their incidence, we believe that elder cadavers that we used would be appropriate as the subject in the present study. Further studies using greater number of cadavers with wider age distribution would be necessary to clarify the process of age-related degenerative changes of the articular cartilage as well as the intraarticular disc of the AC joint. Thirdly, the innervation pattern of AC joint was not taken into consideration, since we focused on the histological changes of articular cartilage and disc. It was reported that the involvement of nerves that innervate AC joint was one of the potential causes of the joint pain [8].

Clinical relevance

Osteoarthritis of the AC joint is one of the common sources of shoulder pain. In addition, the AC joint is commonly involved with inflammatory arthritis, as well as major or minor traumas. Especially, it was known that AC injuries with ligamentous disruption often cause the post-traumatic instability [15]. If the patients complained severe chronic pain for a long time period, resection arthroplasty of the AC joint could be one of the surgical options [12, 18, 19]. Our histological findings concerning both the extent and the localization of degenerative changes might be useful for surgeons to determine the proper amount of bony resection in this procedure.

Conclusion

The lower half of the AC joint is more subject to advanced degeneration of the articular cartilage and the intraarticular disc than the upper half. Therefore, in the surgical treatment of the AC joint osteoarthritis, it might be necessary for surgeons to resect larger amount of bone in the lower part of this joint than in the upper part to remove the severely degenerated tissue.